Breast cancer care amidst a pandemic: a scoping review to understand the impact of coronavirus disease 2019 on health services and health outcomes

Abstract Since the onset of the coronavirus disease 2019 (COVID-19) pandemic, health services for breast cancer (BC) have been disrupted. Our scoping review examines the impact of the COVID-19 pandemic on BC services, health outcomes, and well-being for women. Additionally, this review identifies social inequalities specific to BC during the pandemic. Using the Preferred Reporting Items for Systematic Reviews and Meta-Analyses extension for scoping reviews guidelines, the literature search was conducted using scientific databases starting from March 2020 through November 2021. Studies were identified and selected by two researchers based on inclusion criteria, and the relevant data were extracted and charted to summarize the findings. Ninety-three articles were included in this review. Main themes included are as follows: (i) the impact of COVID-19 on BC services; (ii) the impact of COVID-19 on health outcomes and well-being in women with BC; and (iii) any variation in the impact of COVID-19 on BC by social determinants of health. There were apparent disruptions to BC services across the cancer continuum, especially screening services. Clinical repercussions were a result of such disruptions, and women with BC experienced worsened quality of life and psychosocial well-being. Finally, there were social inequalities dependent on social determinants of health such as age, race, insurance status, and region. Due to the disruption of BC services during the COVID-19 pandemic, women were impacted on their health and overall well-being. The variation in impact demonstrates how health inequities have been exacerbated during the pandemic. This comprehensive review will inform timely health-care changes to minimize long-term impacts of the pandemic and improve evidence-based multidisciplinary needs.


Introduction
The coronavirus disease 2019 (COVID-19) pandemic has impacted millions of individuals around the world [1]. Health services for cancer have been significantly impacted since the emergence of the COVID-19 pandemic, and the majority of cancer centres worldwide have struggled to provide adequate cancer services, including screening and diagnostic services, active treatment, post-treatment care, and outpatient services, due to precautionary measures against COVID-19 and an overwhelmed health system [2][3][4].
Breast cancer (BC) is one of the most common cancers, and women with a diagnosis of BC were classified as vulnerable during the pandemic because of their compromised health status [5]. COVID-19 has also negatively impacted women with BC both physically and psychosocially [6,7]. To inform BC care planning, it would be valuable to better understand how women with BC have being impacted by COVID-19, not only in terms of BC services but also in terms of their well-being, including quality of life (QoL) and their psychosocial health. Such an understanding would inform evidence-based psychosocial care and enable the development of targeted interventions or support services to reduce long-term psychological and physical morbidity from COVID-19 in women with BC.
Evidence is also emerging of potential health inequalities pertaining to COVID-19 [8]. The social determinants of health (SDH) framework details interactions between social and economic factors that may contribute to a greater disruption of health services for certain individuals and negative health outcomes [8,9]. Prior to the pandemic, research on health inequalities for BC identified the following SDH: income, health insurance, education, region, race, and social support [10,11]. Understanding the impact of COVID-19 on BC services and women's well-being within the context of the SDH framework may help identify any patterns of health inequalities pertaining to the pandemic. Therefore, the aim of this scoping review is to examine the impact of COVID-19 on BC services and the health and well-being for women with a diagnosis of BC and how it may vary by SDH.

Methods
This review followed Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) extension for scoping reviews checklist, which defines the necessary items for constructing a scoping review [12] and adhered to the framework methodology of Arksey and O'Malley [13], including the following stages: (i) identifying the research question; (ii) identifying relevant studies; (iii) study selection; (iv) charting the data; and (v) collating, summarizing, and reporting the results.

Identifying the research question
This scoping review was developed to describe the nature, number, and scope of published research articles measuring the impact of COVID-19 on BC services and the health and well-being for women with a diagnosis of BC and how it may vary by SDH.
The following specific research questions were identified to address the aim of the review: (i) How has the COVID-19 pandemic impacted BC services? (ii) How has the COVID-19 pandemic impacted the health and well-being for women living with and beyond BC? (iii) Does the impact of the COVID-19 pandemic on BC services and the health and well-being of women with BC vary according to SDH?

Identifying relevant studies
The literature search was conducted using the following six databases: Embase, PsycINFO, PubMed, CINAHL, Cochrane Library, and Web of Science. The search included only peerreviewed articles published in the English language after 2020. The electronic search strategy included Medical Subject Headings (MeSH), keywords, and their derivatives (pandemic or COVID-19 or coronavirus) and (breast cancer). The search strategy was conducted by a medical librarian in November 2021 (Appendix 1). All articles were downloaded into EndNote, and the duplicates were removed.

Study selection
One reviewer (C.M.) screened all identified articles by titles first. Abstracts were then assessed for eligibility by two researchers (C.M. and C.C.) independently. Detailed inclusion and exclusion criteria are found in Table 1. Eligible abstracts were then sought for full-text retrieval, and full-text articles were reviewed independently (C.M. and C.C.). The review team discussed and resolved differences. Furthermore, alerts were created within each database which will allow for future inclusion of relevant articles.

Charting the data
Data extraction for each full-text article followed corresponding guidelines specific to the study design [14][15][16]. After both researchers (C.M. and C.C.) independently reviewed the selected full-text articles, data were initially extracted from the first five studies and compared by the two reviewers to ensure consistency. The following data were extracted and charted: study design, country, participant characteristics, recruitment method/sample size, time period/phase of lockdown, and main results. Main results were charted to align with the impact of COVID-19 on BC services and/or the impact of COVID-19 on health and well-being separately; for studies that examined and reported on the impact of COVID-19 in relation to SDH, additional data were extracted (e.g. age, race/ethnicity, insurance status, and region).

Collating, summarizing, and reporting
The data from the included studies were collated to provide both descriptive and numerical summary of the findings. To comprehensively understand the impact of COVID-19 on BC, the findings were coded to the three pre-established themes, which correspond with each research question, respectively. A number of sub-themes were then established for each of the three themes: (i) impact of COVID-19 on BC services (screening and diagnostic services, treatment and follow-up care, and telemedicine); (ii) impact of COVID-19 on health outcomes and well-being in women with BC (clinical outcomes, QoL, and psychosocial well-being); (iii) variation in the impact of COVID-19 on BC services and health and well-being by SDH (age, race/ethnicity, insurance status, region, education, marital status, and income). Results are presented narratively by themes and sub-themes in Tables 2-4, and Fig. 1 illustrates a visual summary presentation of the results. Observational studies (retrospective or prospective cohort studies, cross-sectional studies, and case-control studies), qualitative studies, and mixed-methods studies                    Depression and anxiety were positively associated with death anxiety and negatively associated with self-compassion. Selfcompassion was found to be a mediating factor for psychological well-being on death anxiety Psychosocial wellbeing (treatment and follow-up care)    Health and wellbeing (race/ethnicity and insurance) Figure 1 The relationship between COVID-19 and SDH on breast cancer services and health outcomes and well-being.

Screening and diagnostic services
Forty articles identified in the review addressed screening and diagnostic services during COVID-19 (Table 2). BC clinics experienced a reduction in varying breast screening procedures [23,27,28,38,45,49] resulting in a lower number of patients presenting to breast clinics during the pandemic [24]. Patients reported delays in BC screening services [35]. There was a reduction in screening mammograms during the pandemic [18,46,47], especially with the onset of COVID-19 when screening programmes were closed [37,55] and during times with high COVID-19 cases [22]. This reduction was similar for diagnostic mammograms [40,42,43,53], as well as breast biopsies during the pandemic, resulting in fewer BC cases especially among early-stage diagnoses [21]. However, one study found that the methods of detection (i.e. breast imaging versus physical symptoms) during COVID-19 were similar to that of pre-COVID-19 times [50].
Another reason for the reduction in screening appointments was self-cancellations and missed appointments [17]; women were motivated to be screened but balanced the risk of contracting COVID-19 versus the risk of developing BC [32]. For those who did attend in-person screening appointments, women felt safe [41] and the efficacy of those visits was greater than that of pre-pandemic times [20,24]. Several articles addressed the recovery of cancelled and/or missed appointments following COVID-19 lockdown phases [25,42,44,47,48,56]. However, the consequence of accumulated reduction in appointments may impact the diagnostic stage for women [43].
According to nine studies, a decline in the incidence of BC was noted from eight different countries [26,30,31,33,34,39,48,52,54]. No studies found contradictory results. While there was a reduction in overall BC cases during 2020, there were short-term increases in diagnoses in between lockdown phases [34,36]. Late-stage diagnoses increased during the pandemic, but early-stage diagnoses decreased during the pandemic [21,51]. Many women who received a diagnosis of BC were symptomatic [33,34,36,51]; therefore, urgent and symptomatic cases were prioritized during the pandemic [19,29,34,42].

Treatment and follow-up care
Of the 41 articles addressing treatment and follow-up care for BC (Table 2), many countries experienced a drop in in-person visits for services such as surgery, oncology, radiotherapy, and follow-up care (e.g. routine care and rehabilitation) [61, 64-66, 71, 83, 86, 87]. Many studies quantified treatment and appointment delays [70]. On average, the majority of women indicated a delay or change to their regular BC care during the pandemic [5,59,77,78,80,85], and women expressed concerns about such delays on their cancer prognosis [6,60,82,84]. Disruption to appointments and treatments was the result of either the health system [7,71,81] or by choice from the patient [76,79].
The number of BC surgeries declined during the pandemic for a variety of reasons, such as a decrease in referrals, discontinuation in screening programmes, and safety precaution [49,63,71]. Women still experienced delays even after such procedures resumed [57]; however, the types of breast surgery performed during the pandemic did not differ greatly compared to 1-year prior [50]. Additional surgical guidelines and practices include the avoidance of reconstruction surgery, modified mastectomies, shortened length of hospital stay, and outpatient utilization [53,70,72]. With proper prioritization, breast surgery can be safely performed during COVID-19 [68,72]. Several studies found the time to treatment, including surgery, to be longer [49,54,75]; however, one study found the wait time to surgery was lower than pre-pandemic times [58].
There was significant reduction in oncology treatments [73,75]. Decreases in monotherapy administration and increases in oral anti-cancer drugs were common treatment alterations [62]. Moreover, radiation starts were lower during the pandemic, and modification of radiation therapy included regional nodal irradiation and adaptation of radiation therapy [67]. The reasons for delays included screening regulations on availability and accessibility to radiotherapy during the pandemic [69]. Hormonal treatment was more common during the pandemic, while chemotherapy was less common [52,61]. Specifically, one study found an increase in neoadjuvant endocrine therapy [49], and another study found that women treated during COVID-19 were more likely to receive neoadjuvant endocrine therapy [50]. While one study found no difference in the time interval from diagnosis to treatment [51], another study found the time from treatment to surgery increased [74]. Clinicians do not believe that treatment changes should be continued moving forwards from COVID-19 [55].

Telemedicine
Eleven articles included in the review addressed the adaptation of telemedicine for BC services (Table 2). Telemedicine was common for BC management during the pandemic for follow-up appointments, screening for benign disease, second opinion, and general guidance [85], and it proved to be an efficient way to safely monitor BC patients during the pandemic [93]. Even when cancellations recovered after lockdown phases, the use of electronic portals continued to increase, indicating the prolonged uptake of telemedicine among BC patients [56]. Telemedicine was widely accepted by BC patients [91,92,94] and clinicians [55] during the pandemic, and this satisfaction was slightly lower for surgical oncology visits [90]. Women identified telemedicine as a positive alternative to rehabilitation appointments when centres were closed during COVID-19 [7]. Women expressed higher satisfaction for video consultations compared to telephone [88]; however, most would have preferred in-person appointments [89].
Impact of COVID-19 on health outcomes and well-being in women with BC (Table 3) Overall, 46 articles addressed the impact of COVID-19 on health and well-being (Research question 2), and narratives from these articles were organized by sub-themes: clinical outcomes, QoL, and psychosocial well-being.

Clinical outcomes
Fifteen studies discussed the impact of disrupted BC services on clinical outcomes (e.g. late-stage or change in diagnosis) ( Table 3). Despite the decrease in the overall incidence of BC during lockdown phases, late-stage diagnoses increased, indicating more symptomatic and progressed cancer diagnoses [20,30,31]. Even more, the number of BC diagnoses with metastatic lymph nodes significantly increased in 2020, and women reported more tumour-associated symptoms and palpable lumps [19,33,34,51]; researchers predict an increase in BC mortality as a result [36,53,75]. ER-negative and HER2-positive rate was significantly higher during the pandemic [72], and delayed neoadjuvant therapy caused disease progression and delayed surgery may be associated with worsened BC, such as lesions [74]. Women with minimal symptoms were more likely to experience a delay in BC screening; there was a larger decrease in screendetected tumours and diagnoses during the pandemic [26,52]. On the contrary, one study found that BC stage at diagnosis did not differ significantly from pre-COVID-19 to COVID-19 [50].

QoL
Nine studies addressed the QoL of women with BC during the pandemic (Table 3), including physical functioning, social functioning, emotional functioning, and cognitive functioning [87,96]. Fatigue and physical inactivity were mentioned as a consequence of rehabilitation centre closures during the pandemic [7]. Women expressed an increase in responsibility at home and a decrease in social support [97]. Furthermore, women experienced financial distress due to a decrease in household income and an increase in expenditure [82,83,91], which can impact access to food and medicine [95]. Several studies conducted early into the pandemic did not find worsened QoL [81,96]; however, the results may not represent any long-term consequences of the pandemic on women with BC.

Psychosocial well-being
Many studies (n = 30) investigated the impact of COVID-19 on psychological, emotional, and social well-being (Table 3). Disruption to BC care caused treatment-related stress and fear [6,7,80,82,97]. BC patients with heightened depression and anxiety expressed a higher sense of death anxiety [106] and BC recurrence [57,97,101], and one study found that women with heightened anxiety were more likely to cancel their appointments and stay in contact with their BC care team remotely [79]. However, some women reported a higher difficulty to contact their BC care team during the pandemic [96]. Women who received telemedicine during the pandemic were less anxious as they felt assured with continued communication with their BC care team [88], and with telemedicine communication, treatment disruption did not worsen depression and anxiety for women [85].
BC patients expressed depression, along with anxiety and impaired cognitive function [41,73,84,87,91,98,105] during the pandemic, and such psychological impact can be associated with factors such as affected treatment, living alone, comorbidities, immunosuppression, undergoing active treatment, deterioration/metastasis of BC, lacking communication with GP and/or BC care team, and living in high-infection areas [59,100,102,104,105]. Many women expressed worry and anxiety about contracting COVID-19 [60,76,82,91], including fear of COVID-19 transmission in BC facilities [81] and concerns about treatment-related immunosuppression [6]. Women balanced the risk of contracting COVID-19 versus the risk of developing BC [32,41].
Women expressed worsened emotional functioning and vulnerability during the pandemic [60,96,101], and loneliness was another common consequence [6,96,103]. BC patients felt isolated during the pandemic [83], and loneliness was attributed to social isolation and attending treatment visits alone [6]. Insomnia and fatigue were also issues mentioned by women with BC [7,59,87,97,98,100], and some BC patients experienced PTSD during the pandemic [98]. Many women discussed the importance of utilizing coping strategies [6,82]; spirituality and psychological resilience improved patients' fear of cancer recurrence [99].

BC services
There were racial differences with screening appointments (n = 6); Black, Hispanic, and Asian women were more likely to experience a decrease in screening services during the pandemic [17,18,25,27,43,47]. Delays for BC treatment were longer for Black patients compared to White patients, yet this difference was apparent prior to pandemic as well [66]. Additionally, reduction in screening appointments was associated with age, low socio-economic status (SES), limited health insurance, area of residence, and facility type [17,18,25,27,31,35,37]. However, there were contradicting findings for the disruption of screening services based on health insurance status [38]. Additionally, women living in areas of high COVID-19 infection were also more likely to cancel/postpone their screening appointment [45].
For treatment and follow-up appointments (n = 11), women with limited ability to pay (i.e. public health insurance) were likely to experience treatment delays [78]. The following characteristics were associated with specific treatment alterations and delays: older age, marital status, and living in specific regions, such as high-infection areas [49,62,67,68]. For follow-up appointments, younger BC survivors were likely to experience more delays than older BC survivors [5], and variables associated with those who did attend appointments included younger age and lower income [86]. Low educated BC patients were less satisfied with telemedicine [92], and while one study found that older women preferred telemedicine [89], another study found lower satisfaction of telemedicine among women older than 40 years [88].

Health outcomes and well-being
Fewer studies (n = 5) addressed the varying impact of COVID-19 on overall well-being (Table 4). White BC patients reported a higher level of worry than Black BC patients; however, Black BC patients were more likely to experience delays and disruptions prior to the pandemic [80]. Financial difficulties during COVID-19 were more common for minorities and for women with limited health insurance [83]. Likewise, younger age and living further from BC clinic were found to be associated with financial distress [95]. Older women expressed more anxiety due to minimal BC communication [88]; however, younger women expressed higher rumination and emotional vulnerability specific to COVID-19 [60].

Statement of principal findings
There has been a substantial impact on BC services and health outcomes and well-being during COVID-19 occurring across the BC care continuum, from screening services to follow-up care. Therefore, women with a prior diagnosis of BC or awaiting a diagnosis of BC were at risk of disrupted health care and experienced worsened health outcomes during the pandemic, which is comparable to research conducted on all cancer types during the pandemic [108].

Interpretation within the context of the wider literature
The implementation of a triage system helped prioritize highrisk BC patients [109], yet the prioritization for high-risk patients may negatively impact the future prognosis of lowrisk patients, which is consistent with overall cancer research during the pandemic [110]. The overall decrease in BC incidence may be the result of BC screening programmes closures [52], and due to limited capacity and safety precautions, there was also a reduction of in-person appointments for treatment and follow-up care [50,72].
There was a negative impact on QoL and psychosocial well-being which is consistent with general research regarding COVID-19 and cancer [111]. The combination of living with BC during COVID-19 may exacerbate psychosocial distress and death anxiety, and the implementation of supportive care for patients with BC is necessary [6,106]. Historically, pandemics have impacted populations unequally, and this social inequality can exploit populations with chronic disease, including BC [8]. There were evident racial disparities to BC services during the pandemic, which is consistent with research conducted prior to the pandemic [112]. Additional SDH included older age, low SES, health insurance, and area of residence, but due to limited research, more research is needed in this area.

Implications for policy, practice, and research
Since early detection and timely treatment are essential for optimal prognosis and QoL among BC patients [113], research on the long-term clinical impact of the pandemic on BC diagnoses and prognoses is needed. Understanding the influence of COVID-19 on QoL potentially helps enable the development of patient-centred care, tailored intervention strategies, and support services to reduce long-term physical and psychological morbidity [114]. Additionally, the use telemedicine for non-essential needs can optimize BC care post-pandemic [115] and improve psychosocial well-being [88].
The consequences of the pandemic may impact morbidity and mortality for BC globally; therefore, it is important to use this information to implement timely changes to health-care systems to minimize long-term impacts of the pandemic and improve evidence-based multidisciplinary needs, especially for socially disadvantaged groups. Further studies should be conducted across a broader range of countries, and more comparative population-based research on specific sub-themes, such as screening services or clinical outcomes, is required.

Strengths and limitations
The included studies provide a comprehensive scope of the early impact of COVID-19 on various countries. However, it is important to note that most research articles included in this study took place in developed countries and the findings may not be transferable to all countries and several studies had relatively low sample sizes. The majority of the studies included in the review were cross-sectional or retrospective; more prospective studies are needed to understand the longterm impact of the COVID-19 pandemic. Other limitations to this review process include the possibility that some relevant articles may have been missed. Many of the identified and eligible journal articles were only published as an abstract, therefore they were not included. As more information on the topic of COVID-19, BC, and SDH becomes available, the scoping review will be updated.

Conclusion
This scoping review provides a thorough assessment of the impact of the pandemic on BC services and subsequent health outcomes, including QoL, emphasizing the detrimental impact of the pandemic on women with a diagnosis of BC, and for women with pending BC diagnoses. The varying impact to BC care demonstrates how health inequities have been exacerbated during the pandemic by identifying known SDH; therefore, this review has provided evidence of the 'syndemic' relationship between COVID-19, BC, and the SDH.